Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire

Abstract

Traditionally brain function is studied through measuring physiological responses in controlled sensory, motor, and cognitive paradigms. However, even at rest, in the absence of overt goal-directed behavior, collections of cortical regions consistently show temporally coherent activity. In humans, these resting state networks have been shown to greatly overlap with functional architectures present during consciously directed activity, which motivates the interpretation of rest activity as day dreaming, free association, stream of consciousness, and inner rehearsal. In monkeys, it has been shown though that similar coherent fluctuations are present during deep anesthesia when there is no consciousness. Here, we show that comparable resting state networks emerge from a stability analysis of the network dynamics using biologically realistic primate brain connectivity, although anatomical information alone does not identify the network. We specifically demonstrate that noise and time delays via propagation along connecting fibres are essential for the emergence of the coherent fluctuations of the default network. The spatiotemporal network dynamics evolves on multiple temporal scales and displays the intermittent neuroelectric oscillations in the fast frequency regimes, 1–100 Hz, commonly observed in electroencephalographic and magnetoencephalographic recordings, as well as the hemodynamic oscillations in the ultraslow regimes, <0.1 Hz, observed in functional magnetic resonance imaging. The combination of anatomical structure and time delays creates a space–time structure in which the neural noise enables the brain to explore various functional configurations representing its dynamic repertoire.

Author Summary

There has been a great deal of interest generated by the observation of resting-state or “default-mode” networks in the human brain. These networks seem to be most engaged when persons are not involved in overt goal-directed behavior. These networks are also thought to underlie certain aspects of conscious introspection and to be specific to humans. Our paper provides a new explanation for rest state fluctuations by suggesting that they reflect a deeper biological principle of organization and are a consequence of the space–time structure of primate anatomical connectivity. In a computational study using a biologically realistic primate cortical connectivity matrix, we show that the rest state networks emerge only if the time delays of signal transmission between brain areas are considered. The combination of anatomical structure and time delays creates a space–time structure in which the neural noise enables the brain to explore various functional configurations representing its dynamic repertoire. The latter repertoire spans temporal scales of multiple orders of magnitude including scales observed in electric potentials and magnetic fields on the scalp, as well as in blood flow signals. Our results provide a testable explanation of the real-world phenomenon of rest state fluctuations in the primate brain.